Download The origins of multicellular organisms

EVOLUTION & DEVELOPMENT
15:1, 41–52 (2013)
DOI: 10.1111/ede.12013
The origins of multicellular organisms
Karl J. Niklasa,* and Stuart A. Newmanb,*
a
b
Department of Plant Biology, Cornell University, Ithaca, NY, 14853, USA
Department of Cell Biology and Anatomy, New York Medical College, Valhalla, NY 10595, USA
*Author for correspondence (e‐mail: [email protected], [email protected])
SUMMARY Multicellularity has evolved in several eukaryotic lineages leading to plants, fungi, and animals. Theoretically, in each case, this involved (1) cell‐to‐cell adhesion with
an alignment‐of‐fitness among cells, (2) cell‐to‐cell communication, cooperation, and specialization with an export‐of‐
fitness to a multicellular organism, and (3) in some cases,
a transition from “simple” to “complex” multicellularity.
When mapped onto a matrix of morphologies based on
developmental and physical rules for plants, these three
phases help to identify a “unicellular ) colonial ) filamentous
(unbranched ) branched) ) pseudoparenchymatous )
parenchymatous” morphological transformation series that is
consistent with trends observed within each of the three major
plant clades. In contrast, a more direct “unicellular ) colonial
or siphonous ) parenchymatous” series is observed in fungal
and animal lineages. In these contexts, we discuss the roles
played by the cooptation, expansion, and subsequent diversification of ancestral genomic toolkits and patterning modules
during the evolution of multicellularity. We conclude that the
extent to which multicellularity is achieved using the same
toolkits and modules (and thus the extent to which multicellularity is homologous among different organisms) differs among
clades and even among some closely related lineages.
INTRODUCTION
physical laws and processes? Indeed, are the multiple origins of
multicellularity truly independent given that all life ultimately
shared a last common ancestor?
These and other questions about multicellularity have been
addressed in different ways (e.g., Bonner 2012; Niklas 2000;
Kirk 2005; Newman and Bhat 2008, 2009; Newman 2011; Knoll
2011). However, all perspectives share three features: (1) a
comparative approach (because of the multiple origins of
multicellularity, sometimes even within the same clade); (2) a
treatment of how “information” is exchanged among cells and
between cells and their external environment (because coordinated signaling among cells is one of the defining characteristics
of multicellular biology; see Mian and Rose 2011); and (3) a
consideration of functional morphological features (because
these govern energy–mass exchange rates between an organism
and its environment; see Gates 1980).
We address these features as well. However, our primary
objective is to determine, as best as currently possible, whether
the evolutionary trajectory toward multicellularity manifests a
common trend across as well as within clades and, if so, whether
this trend is the result of genomic or physical commonalities
among otherwise diverse organisms. Although we discuss trends
in the fungal and animal clades, our focus is primarily on plants,
which we define broadly as eukaryotic photoautotrophs (Niklas
1997, 2000) to encompass the algae as well as the monophyletic
land plants (embryophytes). This phyto‐centrism is adopted
because (1) multicellularity evolved independently at least six
times in the three major plant clades, which permits extensive
One of the most remarkable events in evolutionary history was
the emergence and radiation of eukaryotic multicellular
organisms (Valentine 1978; Bonner 1998, 2012; Maynard Smith
and Szathmáry 1995; Knoll 2011). Perhaps even more
remarkable is that this “event” occurred independently in
different clades. Estimates of the exact number vary depending
on how multicellular is defined. When defined simply as cellular
aggregation, a conservative estimate is that multicellularity
evolved over 25 times (Grosberg and Strathmann 2007). More
stringent definitions requiring sustained cell‐to‐cell interconnection and communication obtain an estimate of ten eukaryotic
events, that is, once in the Animalia, three in the Fungi (chytrids,
ascomycetes, and basidiomycetes), and six in the three major
plant clades (twice each in the rhodophytes, stramenopiles, and
chlorobionta).
Regardless of the number, the multiple origins of multicellularity and their subsequent consequences evoke a number of
biologically important, but largely unanswered, questions. For
example, do multicellular lineages share a common morphological transformational series? What if any are the selection
barriers to (and the drivers toward) multicellularity? Were
the ancestors of some lineages predisposed to engender multicellular organisms, or is multicellularity the result of random
events leading toward larger organisms. Put differently, are the
morphological motifs that emerge in multicellular lineages the
result of adaptive evolution, or the inevitable consequences of
© 2013 Wiley Periodicals, Inc.
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Vol. 15, No. 1, January–February 2013
interphyletic comparisons, and (2) the origins of plant
multicellularity have been largely neglected in a primarily
zoo‐centric literature. A third reason for focusing on plants is
that all plant clades evolved cell walls that, in contrast to animals,
can restrict intercellular aggregation and communication (and
requires somatic embryogenesis in multicellular plants).
In the following, we (1) characterize multicellular organisms
in terms of intercellular adherence and cell‐to‐cell and cell‐to‐
environment communication, (2) explore the requisite transition
from fitness defined at the level of individual cells to fitness
defined at the level of a truly multicellular entity (Wolpert and
Szathmáry 2002; Michod et al. 2003; Grosberg and Strathmann
2007; Folse and Roughgarden 2012), (3) assess the transition
from simple to complex multicellularity (sensu Knoll 2011),
(4) compare character polarities among the different plant,
fungal, and animal clades, and (5) discuss whether the evolution
of multicellular organisms was instigated by physically based
patterning modules mobilized by shared or unique molecular
toolkits (Newman and Bhat 2009; Hernández‐Hernández et al.
2012).
We will affirm that the evolution of multicellular organisms
typically involved intermediate body plans that were achieved
by similar developmental mechanisms in different lineages, but
not necessarily by mechanisms sharing the same physical or
biochemical components. Much like the plant organs collectively called “leaves,” which evolved independently in different
lineages, multicellularity is a recurrent feature of morphological
evolution that was reached in many different ways. Consequently, the extent to which multicellular organisms are developmentally homologous at the most basic levels requires careful
analyses, particularly since selection acts on functional traits
and not on their underlying generative mechanisms, enabling
different mechanisms to achieve the same functional traits
(Marks and Lechowicz 2006).
EVOLUTIONARY PHASES
Multicellularity has been defined in different ways because of
different taxonomic, developmental, morphological, physiological, or genomic frames of reference. Here, instead of attempting
to define this condition, we focus on two features that enter into
virtually all discussions of multicellular organisms—cell‐to‐cell
adherence, the condicio sine qua non of multicellularity across
all clades, and cell‐to‐cell communication, the basis of multicellular development. However, despite these commonalities,
the cellular and molecular bases of the modes of adherence and
communication differ markedly among clades. Thus, the Ca2þ‐
rhamnogalacturonanic‐dominated composition of the middle
lamella that binds embryophyte cell walls together differs
chemically from the Type‐1 transmembrane cadherin proteins
responsible for animal cell adhesion (Hulpiau and van Roy
2009), or the glycoprotein‐based glues produced by many fungi
(Epstein and Nicholson 2006). Likewise, the intercellular
interconnections in the green alga Volvox differ significantly
from embryophyte plasmodesmata, mammalian gap‐junctions,
or fungal intercellular septal pores that all nevertheless provide
avenues for cell‐to‐cell communication. Just as in cladistics,
“cell‐to‐cell adhesion” and “intercellular communication” can be
thought of as “characters” that assume different “character
states” depending on a lineage’s phyletic legacy.
If cell‐to‐cell adhesion and communication are requisite for
the evolution of multicellular organisms, their basic elements
must have ancestral unicellular character states but not
necessarily manifesting the same functionalities. For example,
molecular analyses identify a diversity of cadherins in the
unicellular choanoflagellate Monosiga brevicollis (a descendent
of the unicellular metazoan progenitor) that likely function in
environment‐responsive intracellular signal transduction, for
example, tyrosine kinase and hedgehog signaling (Abedin and
King 2008). Likewise, adherens junctions tethering metazoan
cells occur in sponge epithelia, albeit in a rudimentary form
(Abedin and King 2010; Suga et al. 2012). One pathway to
fungal multicellularity illustrated by dictyostelid slime molds
(Bonner 2012) shares elements with the evolution of animal
multicellularity. Upon starvation, a developmental cascade is
instigated involving diverse cell‐to‐cell‐to‐substrate adhesion,
for example, membrane bound DdCAD‐proteins facilitating cell
contact play a role similar to that of animal cadherins (Nelson
2008; Bonner 2012). Indeed, the evolution of multicellularity in
the fungi may have been rapid. Using differences in settling
velocities to separate unicellular and clustered Saccharomyces
cerevisiae cells, Ratcliff et al. (2012) isolated isogenic
“snowflake” genotypes with a simple cellular division of labor
and multicellular propagules.
Multicellular organisms can evolve along different pathways
even within the same clade. Consider the chlorobionta. In the
volvocine algae, multicellularity likely evolved by differential
modifications of cell wall layers in a Chlamydomonas‐like
progenitor (Kirk 2005). Specifically, the walls of unicellular
volvocines (e.g., Chlamydomonas) are composed primarily of
hydroxyproline‐rich glycoproteins and are separated into a
structured outer layer and a more amorphous inner layer (Fig. 1).
Among colonial volvocines (e.g., Gonium), adhering cells are
interconnected by struts that preserve the features of the outer
cell wall layer (Fig. 1). However, among multicellular volvocine
algae (e.g., Pandorina and Volvox), the entire plant is surrounded
by a layer that preserves features of the ancestral outer wall
layer by virtue of an unusual pattern of cell division (palintomy)
in which cells undergo multiple divisions without increasing
in total cytoplasmic volume (Herron et al. 2010). High protein
sequence similarities among unicellular and multicellular
volvocines support this scenario; for example, homologs of
the Chlamydomonas outer cell wall protein GP2 occur in
Pandorina and Volvox (Adair and Appel 1989). In contrast, cell
adhesion in the evolutionarily related embryophytes involves a
Niklas and Newman
Fig. 1. Putative evolution of multicellularity in the volvocine algae
(adapted from Kirk 2005). The inner cell wall layer of a unicellular
Chlamydomonas‐like progenitor is modified into an expanded
extracellular matrix (ECM) wherein multicellularity is achieved by
intercellular cytoplasmic strands (e.g., Volvox). The outer cell wall
layer adheres cells in colonial organisms (e.g., Gonium).
middle lamella enriched with pectins, a functionally and
structurally diverse class of galacturonic acid‐rich polysaccharides (Caffall and Mohnen 2009). Chemical modification of
pectins contributes to changing the mechanical properties of cell
walls (Peaucelle et al. 2011; Wolf and Greiner 2012), which
includes cell wall relaxation in concert with indole‐3‐acetic‐acid
(Niklas and Kutschera 2012). Because similar systems are
reported for unicellular green algae (Musatenko 2005), it is
possible that embryophyte cell adhesion evolved by modifications of the fundamental mechanism of cell wall expansion
operating in unicellular progenitors.
Under any circumstances, cell‐to‐cell adhesion in one form or
another participates in the life cycles of nearly every unicellular
organism (e.g., Chlamydomonas gamete‐aggregation) and there
is ample evidence that cell adhesion (and even limited cellular
cooperation) is ancient; for example, the expression of the
flocculation FLO1 gene resulting in S. cerevisiae cell clustering
(Smukalla et al. 2008) and Chlorella (a unicellular green alga)
genome homologues of Arabidopsis auxin receptors (Blanc
et al. 2010). However, although it is a necessary condition for
a multicellular body plan, cell adhesion is insufficient. What
Multicellular origins
43
prevents palmelloid Chlamydomonas, colonial choanoflagellates, and other similar “cellular aggregate” life‐forms from
being multicellular organisms is the failure to constitute
biological entities possessing sustained cell‐to‐cell communication and cooperative interactions among formerly individualized cells (Buss 1987; Bonner 1998), a feature that permits
opportunities for the evolution of cellular specialization (Wolpert
and Szathmáry 2002; Michod et al. 2003). In multicellular plants
and fungi, this capacity may have evolved by the co‐option
of prokaryotic two‐component signaling pathways involving
histidine kinases, response regulators, and in some cases
histidine‐containing phosphotransfer proteins (see Schaller
et al. 2011), which have been identified in a broad spectrum
of eukaryotes including the centric diatom Thalassiosira,
Chlamydomonas, Dictyostelium, a variety of fungi, and
Arabidopsis (Anatharaman et al. 2007). Indeed, the molecular
basis for cell‐to‐cell adhesion and communication may have
evolved simultaneously in some cases; for example, metazoan
tetraspanin‐enriched protein/membrane microdomains participate in cell–cell adhesion and communication as well as
membrane fusion and cell migration (Bailey et al. 2011; Wang
et al. 2012).
But how does a cellular aggregate achieve individuality? One
suggestion is that two evolutionary stages are required—an
alignment‐of‐fitness phase in which genetic similarity among
cells prevents cell–cell conflict and an export‐of‐fitness phase in
which cells become interdependent and collaborate in a
sustained effort (reviewed by Folse and Roughgarden 2012).
The first phase can be achieved by any “unicellular bottleneck”
in an organism’s life cycle, for example, spores or zygotes.
The second phase requires intercellular cooperation sufficient
to shift selection from the level of individual cells to the level of
a multicellular entity that reproduces similar entities with a
heritable fitness, typically followed by some degree of cellular
specialization. Although the separation of soma and a germ‐line
sometimes occurs, obligate sexual reproduction is not required to
override the conflict between the individual and its constituent
cells (Buss 1987; Michod 1997; Nanjundiah and Sathe 2011).
Certainly, in the absence of somatic mutations, the presence of a
zygote in any life cycle assures genetic homogeneity by
providing a unicellular bottleneck regardless of the type of life
cycle (Fig. 2). Likewise, it can be difficult for asexual organisms
to escape the consequences of Muller’s ratchet (the inevitable
accumulation of deleterious mutations). However, asexual
multicellular organisms also experience an alignment‐of‐fitness
by means of unicellular or cloned propagules (Fig. 2).
Likewise, multicellularity is not required for the evolution of
cellular specialization. Unicellular bacteria, algae, yeast, and
amoeba exhibit alternative stable states of gene activity and
even morphology during their life cycles, often as a result of
competing processes, for example, motility versus mitosis. The
origin of cellular differentiation therefore may reside in the
inherent multistability of complex gene regulatory networks
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Fig. 2. Schematics of four contrasting life cycles each with one or more “unicellular bottlenecks” (indicated by an asterisk). Diploid cells and
organisms are shaded; haploid cells and organisms are unshaded. For simplicity, each organism is depicted as a hermaphrodite. (A) The
haplobiontic‐haploid life cycle in which the multicellular phase develops after zygotic meiosis. (B) The haplobiontic‐diploid life cycle in
which the multicellular phase develops from zygotic mitosis. (C) The diplobiontic life cycle containing two multicellular individuals, one
developing after zygotic mitosis and another developing from meiosis. (D) An asexual life cycle in which the multicellular organism and its
unicellular (or cloned) propagules resulting from mitotic cellular division (or fragmentation).
(Laurent and Kellershohn 1999) with somatic or reproductive
functional roles for different cell‐types possibly established ad
hoc by natural selection. Thus, mathematical models indicate
that cellular differentiation can emerge among genetically
identical cells as a response to poor compatibility among
competing physiological processes (Ispolatov et al. 2012). In
more derived lineages, an alignment of fitness can compensate for conflicts of interest among cellular components such
that a division of cellular labor becomes possible and even
necessary.
SIMPLE VERSUS COMPLEX MULTICELLULARITY
Some authors distinguish between “simple” and “complex”
multicellularity (Butterfield 2000; Schlichting 2003). This
distinction has focused recently on whether all cells make
contact with their external environment, or whether some are
internalized (Knoll 2011), for example, unbranched filamentous
morphologies and organisms with tissue systems, respectively.
This difference is important because (1) it is correlated with
differences in cell specialization, energy consumption per
gene expressed, and increases in non‐protein‐coding DNA
(Bonner 2004; Lane and Martin 2010; see, also, Lozada‐Chavez
et al. 2011), (2) it helps to assess the likelihood that a
multicellular organism can evolutionarily revert to a unicellular
state (e.g., a complex multicellular to unicellular transition is
far less likely than a colonial to unicellular transition), and (3) it
helps to identify when a simple multicellular organism
evolutionarily reaches a size or morphology that necessitates
tissue specialization for the bulk transport of nutrients.
Consider the consequence of size on passive diffusion as
shown by a variant of Fick’s law of diffusivity, which estimates
the time required for the concentration of a neutral molecule i
Niklas and Newman
initially absent within a cell to reach 50% of the external
concentration, that is, t0.5 ¼ [V/(APi)] ln (ct¼0/ct¼0.5), where V
is cell volume, A is cell surface area, Pi is the permeability
coefficient of i, and ct¼0 and ct¼0.5 are the concentrations of i at
time zero and at time 50% concentration (Niklas and
Spatz 2012). This formula shows that the time it takes i to
diffuse into a spherical cell from all directions and reach ct¼0.5 is
linearly proportional to cell radius, increases with increasing
volume, and decreases with increasing surface area. Consequently, passive diffusion can be sufficient for the metabolic
demands of small or attenuated cells, filaments, or thin sheets of
cells, but it becomes increasingly insufficient as cells or cell
aggregates increase in size.
Indeed, diffusion is a mode of communication that can drive
cell specialization because increasingly steep gradients in nutrient‐
availability resulting from increasing size or distance can give rise
to a reaction–diffusion (R–D) morphogenetic system. For
example, an Anabena or Nostoc filament is a one‐dimensional
R–D system. Heterocysts manufacture a diffusible inhibitor that
prevents heterocyst formation unless its concentration falls below
a specific threshold (Wilcox et al. 1973; Risser et al. 2012). As the
distance between two heterocysts increases (due to intervening
vegetative cellular divisions), the first undifferentiated cell to be
triggered midway develops into a heterocyst, releases the
inhibitor, and reiterates the process. Analogous R–D systems
operating in two‐ or three‐dimensions are posited for the
development of stomata and root hairs (Torii 2012). Even more
complex examples can be drawn from the evolution of land plants
or extant macroscopic algae. Thus, as early embryophytes evolved
greater height, passive diffusion eventually failed to provide water
to aerial tissues at sufficient rates, thereby requiring bulk water
flow via xylem (Niklas 1997). Likewise, the inner cortex of the
stipes of the great kelp Macrocystis contain specialized “trumpet”
cells that transport photosynthates much like the phloem of
vascular plants (Bruggeln et al. 1985).
Nevertheless, the organization of differentiated cells into two‐
and three‐dimensional patterns, shapes, and forms need not
reflect the immediate consequences of selection (Gilbert 2010).
Although the adaptive advantage of a morphological novelty is
clear (such as in the development of plant and animal vascular
systems), morphological or behavioral novelties can also arise
via phenotypic plasticity (West‐Eberhard 2003; Niklas 2009), or
as a consequence of the inherent physical properties of
embryonic tissues and condition‐dependent developmental
systems (Newman 1994; Newman and Müller 2000; Manning
et al. 2010), only to become assimilated subsequently into the
organism’s developmental program (see, e.g., Palmer 2004).
The former may help to explain why colonial life‐forms often
presage the appearance of multicellularity in some lineages since
phenotypic plasticity among genetically identical cells contributes to fitness (Yokota and Sterner 2010). Likewise, the colonial
body plan has distinct advantages over the unicellular life form;
for example, non‐defective cells can compensate for the defects
Multicellular origins
45
of neighboring cells, or provide resources to other cells that are
then free to specialize.
CHARACTER POLARITIES WITHIN
MULTICELLULAR CLADES
The preceding provides some insight into how unicellular
organisms evolved into simple (and later complex) multicellular
forms because it establishes a hypothetical morphological
transformation series, viz., unicellular ) colonial ) simple
multicellular life forms. For plants, this series can be refined
further based on simple developmental and physical principles
that identify four major body plans, that is, unicellular,
siphonous/coenocytic, colonial, and multicellular (Fig. 3).
Among variants of the plant multicellular body plan, an
unbranched filament of cells is the simplest biophysically
because it requires a single plane of cell division while reducing
drag forces, maximizing light interception, and maintaining a
constant surface area to volume relationship (Niklas 2000).
Further elaboration requires cell division in two and then three
planes of reference, which respectively gives rise to branched
filaments (and the potential for a pseudoparenchymatous
tissue construction) and a parenchymatous tissue construction
(Fig. 3). (We define parenchymatous tissues as those in which
cells can divide in all three planes of reference.) Accordingly,
for plants, the evolution of multicellularity is predicted to
conform to a unicellular ) colonial ) filamentous (unbranched ) branched) ) pseudoparenchymatous ) parenchymatous transformation series. This hypothesis can be evaluated
empirically by mapping the different body plans and tissue
constructions onto current phylogenies for plants, fungi, and
animals. In theory, unicellular, colonial, and simple multicellular
morphologies should map onto ancestral (basal) branches within
each clade, whereas more complex tissue constructions should
map onto more derived branches.
Although recent plant phylogenies inform this hypothesis, the
cladistic resolution within some clades currently lacks sufficient
precision to identify the ancestral body plans even among some
closely related lineages. Perhaps the most difficult clade to
resolve is the red algae (rhodophytes). Molecular data identify
two divergent lineages (one extending from the Porphyridiophyceae and another from the Bangiophyceae) that share the
unicellular Cyanidiophyceae as their sister taxon (Saunders and
Hommersand 2004; Yoon et al. 2009). The porphyridian lineage
contains unicellular, colonial, and what are generally believed to
be more derived multicellular algae, whereas the Compsopogonophyceae contains filamentous algae (Fig. 4). The taxonomic
relationships of the Rhodochaetales and Erythropeltidales
with the Compsopogonophyceae and other related rhodophytes
remain unresolved (Yoon et al. 2009). However, in the
filamentous Bangiophyceae, the immediate ancestral condition
is unicellular and the derived condition in the “floridean” red
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Vol. 15, No. 1, January–February 2013
Karyokinesis and Cytokinesis
Synchronous
No
Siphonous
Colonial
Multicellular
No
Yes
No
Loc
at
Div ion o
isio f
ns
Plane of Division
Indeterminate growth
Symmetry
Cells Adhere
Yes
Symplastic Continuity
No
Unicellular
Yes
1
Yes
unbranched filaments
branched filaments
Simple
Multicellularity
2
pseudoparenchyma
3
parenchyma
Diffuse
Intercalary
Apical
Other
Radial
Dorsiventral
Complex
Multicellularity
Other
Fig. 3. The four major plant body plans shown in bold (unicellular,
siphonous/coenocytic, colonial, and multicellular) configured in a
matrix of the developmental phenomena that give rise to them, two
of which are critical for the evolution of multicellularity: cell‐to‐cell
adherence and cytoplasmic (symplastic) continuity among adjoining
cells. Note that the siphonous/coenocytic body plan may evolve
from a unicellular or a multicellular progenitor. This body plan can
become multicellular directly. The lower panels dealing with the
plane of cell division, localization of cellular division, and symmetry
pertain to the evolution of complex multicellular organisms.
Adapted from Niklas (2000).
algae is pseudoparenchymatous. Molecular analyses of the
monophyletic stramenopiles (Anderson 2004; Maistro et al.
2009) identify three major lineages—the eustigmatophytes,
dictyochophytes, and the pelagophytes (Fig. 5). Within the
eustigmatophyte and the dictyochophyte lineages, the colonial
body plan is derived and the filamentous body plan is observed
only among the most derived genera. The various branches
emerging from the pelagophyte lineage have a complex pattern.
Nonetheless, the unicellular ) colonial ) filamentous (unbranched ) branched) ) pseudoparenchymatous ) parenchymatous transformation series is consistent with current views
regarding the phylogenetic relationships within the brown
algae (phaeophytes) and especially within the yellow‐green
algae (xanthophytes; see Cocquyt et al. 2010) (Fig. 5). Perhaps
the strongest evidence among the three major plant clades
for the unicellular ) colonial ) filamentous (unbranched )
branched) ) pseudoparenchymatous ) parenchymatous
transformational series comes from the molecular phylogenetics
of the monophyletic green plants (chlorobionta) (Lewis and
McCourt 2004; Leliaert et al. 2012). This series occurs within the
“green algae” and within the streptophytes (the charophycean
algae and the embryophytes) (Fig. 6).
In contrast to the plants, the transformational series observed
for the fungi and animals are more truncated. Molecular analyses
indicate that unicellular or siphonaceous (coenocytic) fungi
gave rise to the multicellular condition in the asco‐ and
basidomycetes. Although the monophyletic status of the chytrids
and the lack of resolution at the base of fungal phylogeny make
it difficult to resolve the details of the last common ancestor
(Lutzoni et al. 2004; Schoch et al. 2009) (Fig. 7), the colonial body
plan is absent, whereas multicellular fungi consist of unbranched
filaments that achieve a pseudoparenchymatous tissue construction in asco‐ and basidomycete crown‐taxa, that is, fungal
evolution conforms to a unicellular or siphonous ) unbranched
filament ) pseudoparenchymatous
transformation
series.
Among animals, analyses identify the choanoflagellates as basal
(Fig. 7). The phyletic relationships among the Placozoa,
Ctenophora, and Cnidaria remain uncertain (e.g., Halanych
2004; Dunn et al. 2008). Within the monophyletic choanoflagellates, the unicellular body plan is traditionally interpreted as
ancestral and the colonial body plan as more derived. Although
the phylogenetic relationship between the choanoflagellates and
the Holozoa requires extensive revision, analyses indicate that the
choanoflagellates and Metazoa shared a last common unicellular
ancestor (Carr et al. 2008). Within the Metazoa, the colonial body
plan evolved independently (corals and bryozoans), although it
may be a derived condition. The phyletic relationships among the
Placozoa, Ctenophora, and Cnidaria remain uncertain (e.g.,
Halanych 2004; Dunn et al. 2008). Thus, within the Holozoa, we
see a comparatively simple and direct unicellular ) colonial )
parenchymatous transformational series (Fig. 7). Subsequent,
evolution gave rise to organisms with successively inclusive
morphological motifs, that is, functionally differentiated cell types
(sponges), multilayering (placozoans), interior cavities (ctenophorans, cnidarians), and eventually Bilateria with additional
layers and body cavities (ecdysozoans, mollusks, etc.) and
segments (annelids, etc.) (Newman 2012) (Fig. 8).
The foregoing polarities clearly need to be examined using
finer levels of taxonomic resolution (e.g., Cocquyt et al. 2010) at
the ordinal and family levels. However, they indicate that the
colonial body plan is a consequence of cell adherence mediated
by typically lineage specific molecules with functionalities that
predate the multicellular condition. In the following section, we
argue that other motifs are similarly the result of the automatic
mobilization of physical processes and effects by appropriate
Niklas and Newman
Multicellular origins
47
Fig. 4. Tentative phylogeny of the monophyletic red algae (rhodophytes) based on the phylogenetic analyses of Saunders and Hommersand
(2004; see also Graham et al. 2009, pp. 310–311). The body plans characteristic of terminal branches in the phylogeny are indicated by
schematics (see insert); all groups with multicellular body plans are indicated in bold. The grey arrow indicates that the uppermost branch in the
red algal clade is traditionally placed in the Bangiophyceae.
cell‐interaction‐mediating molecules within the multicellular
state. The self‐organizational capabilities of these “dynamical
patterning modules” (Newman and Bhat 2008, 2009) are
realized in cell clusters arising by aggregation, by failure to
separate after division, or by subdivision of an enlarged cell
(palintomy in plants, cleavage in animals). In evolutionary
terms, genetic uniformity of entities that exhibit developmental
activity can arise therefore before or after the appearance of the
relevant morphogenetic mechanisms (Newman et al. 2006).
Since adaptive selection has little to do with such physically
based morphogenetic effects, framing the origin of multicellular
body plans exclusively in terms of an alignment‐of‐fitness phase
and an export‐of‐fitness phase is perhaps unduly restrictive, an
issue that we return to in our concluding remarks.
Fig. 5. A phylogeny of the monophyletic stramenopiles (brown and golden‐brown algae) based on the analyses of Anderson (2004). The body
plans characteristic of terminal branches in the cladogram are indicated by schematics (see insert); all groups with multicellular body plans are
indicated in bold.
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Fig. 6. A phylogeny of the monophyletic chlorobionta based on the analyses of Lewis and McCourt (2004) and Leliaert et al. (2012). Two
major lineages are recognized: the green algae (chlorophytes) and a lineage containing the charophycean algae and the land plants
(streptophytes). The body plans characteristic of terminal branches in the cladogram are indicated by schematics (see insert); all groups with
multicellular body plans are indicated in bold.
SHARED AND UNIQUE TOOLKITS AND
PATTERNING MODULES
We have emphasized five evolutionary features of multicellular
organisms: cell adhesion, cellular communication, cellular
specialization, tissue pattern formation and morphogenesis,
and “individuality” at the level of a multicellular entity.
Molecular analyses indicate that each of the major multicellular
clades contains a characteristic set of developmental “toolkit”
genes, some of which are shared among disparate lineages (e.g.,
Fig. 7. Redacted phylogeny for the Fungi and Animalia and their respective putative ancestors. The body plans characteristic of terminal
branches in this phylogeny are indicated by schematics (see insert); lineages with multicellular body plans are indicated in bold.
Niklas and Newman
Fig. 8. The elaboration of the animal body plans (shown in bold)
involved additions of successive morphological motifs based on the
mobilization of newly relevant physical effects once the multicellular state evolved. These effects were harnessed by molecules that had
first evolved to serve unicellular functions but that later became
developmental “toolkit” molecules. While aggregates of cells with
the relevant genes would have been capable of generating these
motifs in a heritable fashion, blastulae resulting from cleavage of an
enlarged cell (a “proto‐egg”) would have been genetically uniform
thus exhibiting a greater alignment‐of‐fitness (Newman 2011).
Adapted from Newman and Bhat (2009).
tetraspanin genes in plants, protozoa, insects, fungi, and
mammals; Wang et al. 2012), either by virtue of sharing a last
common ancestor, or as a result of lateral gene flow (e.g., Sun
et al. 2010). However, many are unique to their respective clades
(e.g., cell polarity in plants and animals involves PIN‐ and PAR‐
polarity modules, respectively; Gelder 2009) and some even
differ among closely related lineages (e.g., cell division
mechanisms in unicellular and filamentous ascomycetes; Seiler
and Justa‐Schuch 2010).
A substantial number of toolkit genes in each clade are
developmental transcription factors (DTFs), such as MADS box
gene products in plants and Hox gene products in animals, which,
along with their cis‐acting target sequences on other such genes,
form multistable regulatory networks whose alternative stationary
states determine cell type identity (Furusawa and Kaneko 2002;
Kaneko 2011). Others mediate cell–cell interaction and communication and constitute an “interaction toolkit” (Newman et al. 2009).
Although DTFs cross cell borders only rarely during animal
embryogenesis (Prochiantz and Joliot 2003), they do so more
typically in plants, making them part of the interaction toolkit in
that clade. Other interaction plant toolkit molecules include the
adhesive components described previously and phytohormones
Multicellular origins
49
such as auxin (Niklas and Kutschera 2009; Boot et al. 2012). In
animals, these include cadherins, Notch and Wnt and their
respective ligands, BMP, Hedgehog, and extracellular matrices.
Regardless of the roles they may have played in unicellular
ancestors, these molecules assume entirely new roles in pattern
formation and morphogenesis in the multicellular state, typically
by virtue of the newly relevant physical processes they mobilize at
the mesoscale (Forgacs and Newman 2005; Hamant et al. 2008;
Newman and Bhat 2008, 2009; Manning et al. 2010; Müller 2012).
This has led to animal body plans that are (as noted) variously,
multilayered, hollow or with nested cavities, elongated, segmented
and appendage‐bearing, and to organs with similar morphological
motifs (Fig. 8). Among embryophytes, interaction toolkits are
implicated in branching, phyllotaxy, apical dominance, and the
development of vascular tissues.
Considering the shared and specific interaction toolkits of the
various clades in relation to the physical forces and effects they
mobilize helps explain how phyletically different organisms use
genetically homologous components to construct phenotypically
dissimilar but functionally similar (analogous) structures often
without common ancestors exhibiting the character (Newman
2006). Subtle variations in the physical environment under
which cell aggregation occurs, or minor genetic changes in
adhesion molecules, can result in alternative forms such as solid
or hollow spheroids, filaments, or multilayered tissues. With the
advent of complex multicellularity, the physical and physiological context and microenvironments of distinct subpopulations of
cells (e.g., interior vs. exterior) can yield different developmental
fates. Eventually the conditional effects that contribute to such
morphological variability may become developmentally canalized under selection when their host organisms find suitable
ecological niches. Random gene‐based modifications in body
mass or dimension likewise would alter a priori the rates or
magnitudes of size‐dependent physical phenomena, such as
passive diffusion and mechanical stresses, in ways that would
allow natural selection to filter from a variety of possible forms
those better adapted to available or novel ecological settings.
FUTURE DIRECTIONS
The origination of multicellular organisms required the evolution of mechanisms capable of achieving and maintaining
cellular differentiation temporally as well as spatially. The
unicellular progenitor of each multicellular lineage therefore
must have had the capacity to express alternative states of gene
expression temporally in response to changing environmental
conditions and the pre‐existing regulatory mechanisms responsible for this developmental variability were co‐opted to provide
the capacity to differentiate spatially in the multicellular context.
This new phenotypic context, mediated by preexisting attachment and matrix molecules, led to the mobilization of newly
relevant physical effects and self‐organizing dynamics that
50
EVOLUTION & DEVELOPMENT
Vol. 15, No. 1, January–February 2013
provided the early basis for spatiotemporal regulation in
multicellular organisms (Newman and Bhat 2008, 2009;
Hernández‐Hernández et al. 2012).
The evolutionary expansion of pre‐existing gene families
encoding regulatory proteins in combination with novel physical
and regulatory interactions resulting from such expansions also
played critical roles and may even have driven the evolution of
multicellular complexity (e.g., Feller et al. 2011; Pires and
Dolan 2012), as illustrated by the basic helix‐loop‐helix (bHLH)
protein family involved in diverse cellular developmental
processes in both plants and animals (reviewed by Feller et al.
2011). Indeed, many intracellular functions involve bHLH–
bHLH interactions as well as synergistic interactions with other
regulatory proteins, such as MYB, to form complexes that either
repress or activate the expression of sets of target genes (Ramsay
and Glover 2005; Feller et al. 2011). Future research is required
to identify these targets and to determine their participation in
developmental processes. However, as noted, it is critical to
determine the extent to which the details of transcription factor
regulation and gene network architecture carry over from
one organism to another, since sequence homologies do not
necessarily imply the conservation of function. Likewise,
functional homologies are not invariably the result of genomic
or developmental homology, as is evident from the broad
spectrum of molecules providing cell adhesion and intercellular
communication. Nevertheless, we believe that future research
will show that that three vastly different plant clades achieved
multicellularity along a similar morphological transformation
series, e.g., unicellular ) colonial or siphonous ) filamentous
(unbranched ) branched) ) pseudoparenchymatous ) parenchymatous.
Finally, we have side stepped the question of whether
multicellularity confers any selective advantage. Certainly, the
current abundance of multicellular organisms gives the impression that it does. Likewise, it allows an organism to exceed the
size limits imposed by passive diffusion. Although we are
sympathetic to the notion that major evolutionary innovations
will not be retained within a lineage if they are incompatible with
survival, it is not always the case that every transition requires a
large or even measurable advantage (Grosberg and Strathmann
2007), nor is it the case that phenotypic responses to selection
invariably are in the direction of an adaptive advantage
(Bonduriansky and Day 2009). Thus, a recent theoretical model
for filamentous bacteria shows that strains with the same fitness
can produce genotypes differing in cell‐number as a result of
differences in cell division and death rates, or as a result of
changes in the environmental carrying capacity (Rossetti
et al. 2011). This model, which has empirical support, also
shows that differences in fitness attributable to morphology
are not required a priori for the evolution of life cycles with
multicellular entities (Rossetti et al. 2011), although advantages
may arise subsequently (Koschwanez et al. 2011). The retention
of multicellularity in some lineages therefore may reflect
“diffusion from the left (unicellular) wall of life” (sensu
Gould 1989; Marcot and McShea 2007). Indeed, although
examples of a unicellular organism descending from a
multicellular organism are known (Velicer et al. 1998; Schirrmeister et al. 2011), once an organism passes through the export‐
of‐fitness phase and achieves complex multicellularity, its
capacity for contingent evolutionary reversion to a simpler state
is reduced for reasons that have little or nothing to do with
selection on fitness.
Acknowledgments
The authors thank Drs. Randy Wayne and Dominick J. Paollilo, Jr.
(Cornell University), Dr. Michael Christianson (University of California, Berkeley) and two anonymous reviewers for helpful suggestions
and acknowledge support from the College of Agriculture and Life
Sciences, Cornell University, and from the New York Medical College,
Valhalla. This article is dedicated to Prof. John T. Bonner (Princeton
University) for his seminal contributions to understanding the origins of
multicellularity.
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